Characters of the female gonad and the phylogeny of Platyhelminthes

The female gonad of Platyhelminthes shows a wide variability in its anatomical and cellular organization and submicroscopic structure, and some characteristics may be useful for elucidating the questioned monophyly of some taxa and reconstructing the phylogenetic tree of the group. The morphological characters of the female gonad have been subdivided into three levels: macroscopic, microscopic and ultrastructural, and some examples with potential phylogenetic value are presented for each level. This revised version was published online in July 2006 with corrections to the Cover Date.     

The female gonad in two species of Microplana (Platyhelminthes,Tricladida, Rhynchodemidae): Ultrastructural and cytochemical investigations

The female gonad of the land planarians Microplana scharffi and Microplana terrestris consists of two small germaria located ventrally in the anterior third of the body and of two ventro‐lateral rows of oblong vitelline follicles distributed between the intestinal pouches. Both these structures are enveloped by a tunica composed of an outer extracellular lamina and an inner sheath of accessory cells. Oocyte maturation is characterized by the appearance of chromatoid bodies and the development of endoplasmic reticulum and Golgi complexes. These organelles appear to be correlated with the production of egg granules with a fenestrated/granular content of medium electron density, about 4–5 μm in diameter, which remain dispersed in the ooplasm of mature oocytes. On the basis of cytochemical tests showing their glycoprotein composition, and their localization in mature oocytes, these egg granules have been interpreted as yolk. In the vitelline follicles, vitellocytes show the typical features of secretory cells with well‐developed rough endoplasmic reticulum and Golgi complexes involved in the production of eggshell globules and yolk. The eggshell globules, which appear to arise from repeated coalescences of two types of Golgi‐derived vesicles, contain polyphenols and, when completely mature, they measure about 1–1,2 μm in diameter and show a meandering/concentric content pattern as is typical of the situation observed in most Proseriata and Tricladida. Mature vitellocytes also contain a large amount of glycogen and lipids as further reserve material. On the basis of the ultrastructural features of the female gonad and in relation to the current literature the two species of rhynchodemids investigated appear to be closely related to the freshwater planarians belonging to the family Dugesiidae. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Ultrastructure of the female gonad of two temnocephalids (Platyhelminthes,Rhabdocoela)

The female gonad of Temnocephala dendyi and T. minor consists of a single germarium and two rows of vitellaria. It is enveloped by an extracellular lamina and accessory cells. Accessory cells are only peripherally located in the germarium while their cytoplasmic projections also fill the spaces between vitellocytes in the vitellarium. The main feature of oocyte maturation is the appearance of chromatoid bodies and the development of rough endoplasmic reticulum (R.E.R.) and Golgi complexes which appear to be correlated with the production of double-structured egg granules. The egg granules, which are localized in the cortical cytoplasm of mature oocytes, contain glycoproteins, are devoid of polyphenols and are similar in structure and composition to the cortical granules observed in some Digenea and Monogenea. Vitellocytes are typical secretory cells with well-developed R.E.R. and Golgi complexes which are involved in the production of shell globules and yolk. The multigranular pattern and the polyphenolic composition of the shell globules of the temnocephalids investigated are similar to those observed in other rhabdocoels, and in some Prolecithophora and Neodermata. This feature may represent a synapomorphy shared by these taxa. This revised version was published online in July 2006 with corrections to the Cover Date.     

Ultrastructural and cytochemical studies of the female gonad of Prorhynchus sp. (Platyhelminthes,Lecithoepitheliata)

The female gonad of Prorhynchus is heterocellular (neoophoran organization) and consists of an unpaired, elongate germovitellarium enveloped by a finely granular extracellular lamina. It is composed of a posterior germinative area where early oocytes are randomly associated with differentiating vitellocytes and a growth area with follicular organization. In each follicle a single oocyte is surrounded by a layer of vitellocytes. By electron microscopy, the oocytes showed features typical of non-vitellogenic germ cells; they had chromatoid bodies, annulate lamellae, lipid droplets and R.E.R. and Golgi complexes producing small granules with a multilamellar pattern. Vitellocytes showed features typical of secretory cells with the R.E.R. and Golgi complex developed to a great extent and involved in the production of type A and type B globules, respectively. We speculate that type A globules are shell-globules and type B globules are yolk. The structure, composition and role of vitellocyte globules of Prorhynchus are compared with those of homologous inclusions from other Platyhelminthes.Abbreviations A type A globule - B type B globule - ECL extracellular lamina - GC Golgi complex - L lipid - RER rough endoplasmic reticulum - O oocyte - V vitellocyte     

The evolution of gonad expenditure and gonadosomatic index (GSI) in male and female broadcast‐spawning invertebrates

Sedentary broadcast‐spawning marine invertebrates, which release both eggs and sperm into the water for fertilization, are of special interest for sexual selection studies. They provide unique insight into the early stages of the evolutionary succession leading to the often‐intense operation of both pre‐ and post‐mating sexual selection in mobile gonochorists. Since they are sessile or only weakly mobile, adults can interact only to a limited extent with other adults and with their own fertilized offspring. They are consequently subject mainly to selection on gamete production and gamete success, and so high gonad expenditure is expected in both sexes. We review literature on gonadosomatic index (GSI; the proportion of body tissue devoted to gamete production) of gonochoristic broadcast spawners, which we use as a proxy for gonad expenditure. We show that such taxa most often have a high GSI that is approximately equal in both sexes. When GSI is asymmetric, female GSI usually exceeds male GSI, at least in echinoderms (the majority of species recorded). Intriguingly, though, higher male GSI also occurs in some species and appears more common than female‐biased GSI in certain orders of gastropod molluscs. Our limited data also suggest that higher male GSI may be the prevalent pattern in sperm casters (where only males release gametes). We explore how selection might have shaped these patterns using game theoretic models for gonad expenditure that consider possible trade‐offs with (i) somatic maintenance or (ii) growth, while also considering sperm competition, sperm limitation, and polyspermy. Our models of the trade‐off between somatic tissue (which increases survival) and gonad (which increases reproductive success) predict that GSI should be equal for the two sexes when sperm competition is intense, as is probably common in broadcast spawners due to synchronous spawning in aggregations. Higher female GSI occurs under low sperm competition. Sperm limitation appears unlikely to alter these conclusions qualitatively, but can also act as a force to keep male GSI high, and close to that of females. Polyspermy can act to reduce male GSI. Higher male than female GSI is predicted to be less common (as observed in the data), but can occur when ova/ovaries are sufficiently more resource‐intensive to produce than sperm/testes, for which some evidence exists. We also show that sex‐specific trade‐offs between gonads and growth can generate different life‐history strategies for males and females, with males beginning reproduction earlier. This could lead to apparently higher male GSI in empirical studies if immature females are included in calculations of mean GSI. The existence of higher male GSI nonetheless remains somewhat problematic and requires further investigation. When sperm limitation is low, we suggest that the natural logarithm of the male/female GSI ratio may be a suitable index for sperm competition level in broadcast spawners, and that this may also be considered as an index for internally fertilizing taxa.     

Ultrastructural and cytochemical aspects of the female gonad of Geoplana burmeisteri (Platyhelminthes, Tricladida, Terricola)

The ultrastructure of the female gonad of the land planarian Geoplana burmeisteri was investigated by means of electron microscopy and cytochemical techniques. It consists of two small germaria located ventral to the intestine and of two irregular, lateral rows of vitelline follicles, both enveloped by a tunica composed of an extracellular lamina and an inner sheath of accessory cells. Accessory cell projections completely surround developing oocytes and vitellocytes. The main feature of oocyte maturation is the appearance of chromatoid bodies and the development of the rough endoplasmic reticulum (RER) and Golgi complexes. These organelles appear to be correlated with the production of egg inclusions of medium electron density, about 1.5-1.8 microm in diameter, which remain scattered in the ooplasm of mature oocytes. On the basis of cytochemical tests demonstrating their glycoprotein composition, these inclusions were interpreted as residual yolk globules. Vitellocytes are typical secretory cells with well-developed RER and Golgi complexes that are mainly involved in the production of yolk globules and eggshell globules, respectively. Eggshell globules appear to arise from repeated coalescence of small Golgi-derived vesicles and, at an intermediate stage of maturation, show a multigranular pattern. Later, after vesicle fusion, they reach a diameter of 1.3-1.6 microm when completely mature and show a meandering/concentric pattern, as is typical of the situation seen in most Proseriata and Tricladida. The content of yolk globules is completely digested by pronase, while the content of eggshell globules is unaffected. Mature vitellocytes contain, in addition, a large quantity of glycogen and lipid droplets as further reserve material. On the basis of the ultrastructural characteristics of the female gonad described above and in relation to the current literature, we conclude that G. burmeisteri appears to be more closely related to the freshwater triclads, in particular to members of the Dugesiidae, than to the marine triclads.     

The female genital system of Ooperipatellus decoratus (Onychophora, Peripatopsidae): an ultrastructural study

The female genital system of the oviparous peripatopsid Ooperipatellus decoratus consists of an ovary, oviducts equipped with receptacula seminis and additional pouches, uteri, and a vagina. It is examined using transmission and scanning electron microscopy. The ovary is made up of paired ovarian tubes united anteriorly and posteriorly and differentiated into a sterile dorsal part and a fertile ventral part with exogenous oocytes. Fertilization presumably occurs in the oviducts once the oocytes pass the receptaculum seminis. Although the receptacula seminis have been reported to occur in juvenile O. decoratus females only, the present study reveals that they are present in adult females as well. Their wall consists of a cuboidal epithelium covered with a thin collagen-muscle layer. The additional pouches are projections of the oviducts facing the receptacula seminis. They are distally closed to the haemocoel by a flattened epithelium and lack external muscle cells. A thin collagen layer is only found proximally. The uteri are characterized by a columnar epithelium with folded cell membranes allowing extension of the uteri, thus facilitating the passage of the large uterine eggs towards the vagina. Another dominating feature of the uteri is a distally increasing secretory production, which probably contributes to chorion development. Cilia occurring along the entire length of the uteri are considered to assist in the transport of eggs towards the vagina.     

Origin of the gonad in the juvenile of a solitary ascidian, Ciona intestinalis

In the just-metamorphosed juveniles of Ciona intestinalis, a round mass of tissue debris derived from the resorbed tadpole tail is situated in the broad space enclosed by the peritoneal membrane and the epidermis around the ventral side of the esophagus. In living juveni es, the origin of the gonad rudiment was traced back to the mass of tissue debris. Electron microscopically, the round mass was a clump of irregular-shaped phagocytotic cells engulfing degenerated cell fragments. On the surface of the cell clump, a small number of singly occurring round cells were found and identified as primordial germ cells on the basis of morphological continuity to obvious germ cells in later stages. Presence of nuage around the nucleus characterized the germ cells. In a few days the germ cells assembled to form a solid slender body (gonad rudiment) together with smaller somatic cells. The gonad rudiment left the space around the esophagus, moving into the narrow mesenteric space connecting the stomach and intestine on the fourth day after metamorphosis. It gradually increased in size by proliferation of the germ cells and somatic cells. The solid gonad rudiment changed into an oval vesicle with an eccentrically located cavity on about the seventh day after metamorphosis. The vesicle comprised a thinner wall made of a simple epithelium without germ cells and a thicker wall containing germ cells and somatic cells.     

Ultrastructural investigations of the female genital system of Epiperipatus biolleyi ( Bouvier 1902) (Onychophora,Peripatidae)

Brockmann, C., Mummert, R., Ruhberg, H. and Storch, V. 1999. Ultrastructural investigations of the female genital system of Epiperipatus biolleyi (Bouvier 1902) (Onychophora, Peripatidae). — Acta Zoologica (Stockholm) 80: 339–349. The female genital system of the neotropical peripatid Epiperipatus biolleyi was examined using transmission and scanning electron microscopy. Special attention is given to the two accessory organs of the paired oviducts: the receptacula seminis and the ovarian funnels (Ovarialtrichter). The latter occur only in the Peripatidae, whereas receptacula seminis may also be present in the Peripatopsidae, the only other family in the Onychophora. The ovarian funnels of E. biolleyi are thin-walled and closed from the haemocoel. This trait has also been reported from Epiperipatus trinidadensis, Macroperipatus torquatus, and Eoperipatus weldoni, whereas other peripatids have ovarian funnels which have been reported to open into the haemocoel. The occurrence of artificially opened ovarian funnels, caused by tissue rupture during specimen preparation, is discussed. The presence of spermatozoa both in the receptaculum seminis and in parts of the uterus of the female examined in this study supports the hypothesis that in E. biolleyi insemination of juvenile females occurs directly via the genital opening. The female contained one unstalked cleavage embryo in each uterus horn. Two features of the uterus were found to be unique to E. biolleyi: (1) a second cell layer overlying the uterine epithelium with a pronounced secretory activity (2) embryos are enclosed in a noncellular coat interspersed with numerous transport vesicles.     

Seasonal variation in the oviduct of female Agkistrodon piscivorus (Reptilia:Squamata): An ultrastructural investigation

The annual oviductal cycle of the Cottonmouth, Agkistrodon piscivorus, is described using electron microscopy. This is only the second such study on a snake and the first on a viperid species. Specimens were collected in reproductive and nonreproductive condition throughout the year and five ultrastructurally unique regions were recognized: the anterior infundibulum, posterior infundibulum, glandular uterus, nonglandular uterus, and vagina. Except for the anterior infundibulum and vagina, which exhibit no seasonal variation in ultrastructure, the oviduct becomes highly secretory at the start of vitellogenesis. This includes the entire luminal border of the uterus, the tubular glands of the glandular uterus, and the luminal border and sperm storage tubules of the posterior infundibulum. The secretory materials produced in the oviduct vary among regions of the oviduct, and also can vary among time periods in the same region of the oviduct. Variation is especially evident in the sperm storage tubules. Secretory activity in the sperm storage tubules ceases after ovulation, but the tubular glands of the glandular uterus remain secretory until parturition, at which time secretory activity in the varying sections of the oviduct decreases dramatically. After parturition, the oviduct remains in a dormant state until the next reproductive season. The seasonal variation in oviducal morphology mirrors the temperate primitive reproductive cycle known for some pitvipers. Uterine glands of A. piscivorous are more similar in secretory activity to those of an oviparous lizard than a viviparous colubrid snake, suggesting variation in uterine gland morphology between snakes of different families. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Reproductive competition promotes the evolution of female weaponry

Secondary sexual traits in females are a relatively rare phenomenon. Empirical studies have focused on the role of male mate choice in their evolution; however, recently it has been suggested that secondary sexual traits in females are more likely to be under selection via reproductive competition. We investigated female competition and the influence of female phenotype on fitness in Onthophagus sagittarius, a species of dung beetle that exhibits female-specific horns. We compared reproductive fitness when females were breeding in competition versus breeding alone and found that competition for breeding resources reduced fitness for all females, but that smaller individuals suffered a greater fitness reduction than larger individuals. When females were matched for body size, those with the longest horns gained higher reproductive fitness. The fitness function was positive and linear, favouring increased horn expression. Thus, we present evidence that female body size and horn size in O. sagittarius are under directional selection via competition for reproductive resources. Our study is a rare example of female contest competition selecting for female weaponry.     

The evolution of female mole ovotestes evidences high plasticity of mammalian gonad development

Previous studies of the reproductive biology and genetics of European moles (Talpa spp.) showed that all females of these species have ovotestes (gonads with testicular and ovarian tissue) instead of normal ovaries, a unique specialization among mammals. Females are fertile as their ovarian tissue is fully functional. Testicular tissue is abnormal and sterile, but produces high levels of testosterone. This phenomenon also characterizes other talpid species from Europe and North America. To study the origin of this singular reproductive specialization, we examined the gonads of several female specimens belonging to two critical taxa. Although large Japanese moles (Mogera wogura) posses ovotestes, greater Japanese shrew moles (Urotrichus talpoides) are characterized by normal ovaries. The results fit parsimoniously with a recent phylogenetic study that places Urotrichus relatively basal in the talpid tree and separate from the American shrew mole. Parsimony reconstruction on alternative phylogenetic hypotheses clearly indicates that reversal(s) must have occurred and suggests that a relatively simple genetic mechanism must be associated with the evolution of female hermaphroditism in moles.     

Inter-annual variation in the gonad cycle of the mackerel icefish

Spawning by Antarctic fish is generally considered to be seasonal and restricted to a brief period during the autumn and winter. Arising from this it has been assumed that the gonadal maturation cycle is also closely associated with the time of year. The gonad maturation cycle of the mackerel icefish Champsocephalus gunnari was investigated using data collected during research surveys and from sampling the commercial fishery. Spawning appears to occur at the same time each year, but the timing of gonadal development is subject to a considerable inter-annual variation. The implications of this variation are discussed with respect to feeding conditions.     

The evolution of female genitalia

Female genitalia have been largely neglected in studies of genital evolution, perhaps due to the long‐standing belief that they are relatively invariable and therefore taxonomically and evolutionarily uninformative in comparison with male genitalia. Contemporary studies of genital evolution have begun to dispute this view, and to demonstrate that female genitalia can be highly diverse and covary with the genitalia of males. Here, we examine evidence for three mechanisms of genital evolution in females: species isolating ‘lock‐and‐key’ evolution, cryptic female choice and sexual conflict. Lock‐and‐key genital evolution has been thought to be relatively unimportant; however, we present cases that show how species isolation may well play a role in the evolution of female genitalia. Much support for female genital evolution via sexual conflict comes from studies of both invertebrate and vertebrate species; however, the effects of sexual conflict can be difficult to distinguish from models of cryptic female choice that focus on putative benefits of choice for females. We offer potential solutions to alleviate this issue. Finally, we offer directions for future studies in order to expand and refine our knowledge surrounding female genital evolution.     

豌豆潜蝇姬小蜂雌蜂触角感器的扫描电镜观察

应用扫描电镜观察豌豆潜蝇姬小蜂Diglyphus isaea Walker雌蜂触角感器,包括Bhm氏鬃毛、感觉孔、单孔毛状感器、多孔片状感器、锥形乳头状感器、厚壁化学感器、薄壁化学感器和毛状感器8种感器,分别对这8种感器的形态特征进行详细描述,并推测其可能的功能;还对有关的潜蝇姬小蜂生物学特性做深入的分析和讨论。     

The abdomen of a free-living female of Strepsiptera and the evolution of the birth organs

Mengenillidae is a small, basal family of Strepsiptera, mainly characterized by free-living females in contrast to the endoparasitic females of Stylopidia. Here, we describe external and internal structures of the female abdomen of Eoxenos laboulbenei (Mengenillidae). The external morphology was examined and documented using microphotography. Internal structures were reconstructed three-dimensionally using a μCT-data set. The morphologically simplified abdomen comprises 10 segments. The integument is weakly sclerotized and flexible. Spiracles are present dorsolaterally on segments I–VII. Segment VII bears the posteroventral birth opening and the small abdominal segment X carries the anus at its apex. Numerous eggs float freely in the hemolymph. The musculature of segments I–IV is composed of ventral and dorsal longitudinal muscle bundles, strongly developed paramedial dorsoventral muscles and a complex meshwork of small pleural muscles, with minimal differences between the segments. Segments V–X contain more than 50 individual muscles, even though the musculature as a whole is weakly developed. Even though it is not involved in processing food, the digestive tract is well-developed. Its postabdominal section comprises a part of the midgut and the short hindgut. The midgut fills a large part of the postabdominal lumen. The lumina of the midgut and hindgut are not connected. Five or six nodular Malpighian tubules open into the digestive tract at the border region between the midgut and hindgut. The birth organ below the midgut releases the primary larvae after hatching via the birth opening at segment VII. It is likely derived from primary female genital ducts. The presence of six additional birth organs of segments I–VI are de novo formations and a groundplan apomorphy of Stylopidia, the large strepsipteran subgroup with endoparasitic females. The loss of the primary birth organ of segment VII is an apomorphy of Stylopiformia (Stylopidia excl. Corioxenidae).     

A new interpretation of the female genitalia in Macrocyclops albidus (Copepoda, Cyclopidae)

The female genital structures of Macrocyclops albidus (Cyclopidae, Eucyclopinae) were studied using light and electron microscopy. The results confirm that the exterior genital area shows only a copulatory pore, located anteromedially on the ventral face of the genital double-somite, and paired gonopores (not directly visible), situated laterally under the P6 plates. An internal seminal receptacle, composed of several parts, is connected to the gonopores by ventro-lateral cuticular extensions or seminal ducts. The lateral site of communication shows a complex set of connections between the seminal receptacle and the oviducts (via the egg-laying ducts). The structure until now designated as ‘transverse ducts’, visible by transparency on the ventral face, is in fact constituted of internal cuticular thickenings resulting of the fusion of the 6th thoracic somite and the 1st abdominal somite forming the genital double-somite and appearing externally as a part of the suture line; the term ‘suture cord’ is proposed to designate it. The functioning of the system is explained.     

Histological study of the development and sex differentiation of the gonad in the European eel

The histological structure of the gonads was studied in yellow eels sampled from a coastal lagoon and from stocks reared in an aquaculture plant showing different sex ratios. Gonad development related to body size rather than to age and underwent an intermediate stage characterized by a structure of an early testis but containing oogonia and oocytes. This gonad was called the Syrski organ and the stage juvenile ambisexual. Ovaries were found in eels from 22–30 cm in length, possibly derived from undifferentiated gonads or from Syrski organs. Fully differentiated testes were found in eels >35 cm, derived from Syrski organs. These observations support the results of previous research. From elvers and in eels up to 15–16 cm in length, growth of the gonadal primordium is due to primordial germ cell migration. In eels > 15 cm multiplication of primordial cells begins. Oogonial clones were found in eels > 18 cm in length, whilespermatogonium B clones were observed in eels >30 cm in length. The dynamics of sex differentiation was different among stocks with different ultimate sex ratios: ovaries were found in shorter eels in stocks with a prevalence of females, in longer eels in stocks with a prevalence of males. This result supports the hypothesis of a metagametic (environmental) sex determination. The somatic cells in contact with germ cells and those in the interstitium appeared early during gonad development and preceded germ cell differentiation. This suggests that somatic cells are the targets of the environmental factors influencing sex differentiation.     

Sperm aggregations in female Agkistrodon piscivorus (Reptilia:Squamata): a histological and ultrastructural investigation

Upon copulation in female Agkistrodon piscivorus, sperm migrate up the oviduct to sperm storage tubules (SSTs) in the posterior infundibulum. The epithelium of the SSTs is composed of ciliated and secretory cells and differs ultrastructurally from that of the epithelium lining the lumen of the posterior infundibulum. Sperm pass through an area composed primarily of ciliated cells at the opening of each gland before aligning themselves in parallel arrays with their nuclei facing an area composed primarily of secretory cells at the base of the tubules. Sperm are also found embedded inter- and intracellularly in the SSTs. The secretory vacuoles in the SSTs become highly electron dense after the start of the fall mating season along with the synthesis of lipid droplets. Histochemical analysis reveals that the alteration in secretory material density is caused by the production of neutral carbohydrates. Some sperm remain in aggregates in the nonglandular section of the posterior uterus until the time of ovulation. However, ultrastructural evidence indicates these sperm degrade before ovulation. Therefore, sperm in posterior aggregates have no role in fertilization of ovulated ova. The data presented here support the hypothesis that infundibular sperm storage is the mode that snakes utilize to sequester viable sperm until ovulation.     

The evolution of alternative cryptic female choice strategies in age-structured populations

Abstract.— Cryptic female choice is a potentially important aspect of the sexual selection process. According to the theory of sexual dialectics, postcopulation manipulation of relative male fertilization success can provide an avenue by which females can circumvent attempts by males to control female reproduction. Here I use stochastic models to investigate the evolution of cryptic female choice in populations with and without age structure. In populations without age structure, cryptic female choice will evolve only when (1) precopulatory mate choice by females is inefficient, (2) variation in male fitness is correlated with a trait upon which a female can base her choice of mates, and (3) the cost of multiple mating is not too high. In populations with age structure, similar conditions apply. However, selection sometimes favors females that employ alternative strategies of female choice at different ages. These results help to define the types of biological systems in which we should expect to see the evolution of cryptic female choice. They also illustrate that the evolution of choice strategies in females may be complex and may mirror in some important respects the evolution of alternative mating tactics in males.